Phenotypic Plasticity 11 in the Fossil Record Adrian M. Lister The Natural History Museum, London CONTENTS 11.1 Introduction ..................................................................................................268 11.2 Identifying Phenotypic Plasticity in the Fossil Record ................................269 11.2.1 Correlation with Paleoenvironmental Variation ...............................269 11.2.1.1 Analogy with Living Relatives .......................................... 271 11.2.1.2 The Pattern of Variation .................................................... 273 11.2.1.3 Parallel Change across Species .......................................... 275 11.2.2 Ontogeny and Growth ....................................................................... 275 11.2.2.1 Magnitude of Change ......................................................... 275 11.2.2.2 Relative Growth ................................................................. 276 11.2.2.3 Growth Influenced by Substrate ........................................ 276 11.2.3 Behavioral Traces .............................................................................277 11.2.4 Speed and Reversibility of Change ...................................................277 11.2.5 Variation within a Single Genetic Individual ................................... 278 11.2.5.1 Variation of Growth Rate ................................................... 278 11.2.5.2 Bilateral Asymmetry .........................................................279 11.2.5.3 Variation within Colonial Organisms ................................279 11.2.5.4 Behavioral Variation of a Single Individual ......................280 11.2.6 Direct Genetic Evidence ...................................................................280 11.2.7 Summary .......................................................................................... 281 11.3 Phenotypic Plasticity and Evolution ............................................................. 281 11.3.1 Production and Maintenance of Adaptive Plasticity ........................ 281 11.3.2 Plastic Variation, Selection, and Assimilation .................................283 11.3.3 Guiding the Direction of Evolution ..................................................283 11.3.4 Behavioral Plasticity .........................................................................287 11.3.5 Inhibition of Evolution and Extinction .............................................290 11.4 Conclusion .................................................................................................... 291 Acknowledgments ..................................................................................................292 References ..............................................................................................................292 DOI: 10.1201/9780429343001-11 267 268 Phenotypic Plasticity & Evolution 11.1 INTRODUCTION Phenotypic plasticity, the ability of an individual organism to express different phe- notypes in response to varying environmental conditions, is ubiquitous across life’s diversity. It is also increasingly recognized as fundamental to the survival and adap- tive capacity of organisms, as well as forming an integral part of the evolutionary process (West-Eberhard 2003; see also Pfennig 2021 and Sultan 2021 in this volume). We can suppose as a working assumption that what is true today must have also been true for organisms in the past (Chauffe and Nichols 1995). While almost all research on phenotypic plasticity has been based on living organisms, the fossil record has the potential to test models of biological processes with resources not amenable to the biology of the present-day: • Long time-series to trace phenotypic change and variability on timescales ranging from 100 to 109 years • Extinct relatives of living taxa, as models of ancestral phenotype and variation • Quantification of diversification and extinction in clades through time Evolutionary hypotheses that could in principle be tested in the fossil record include the origin of adaptive plasticity in heterogeneous environments; the reduction of plasticity in more stable environments; the role of plasticity (including behavioral plasticity) in promoting and guiding evolution and dispersal; and the part played by plasticity in major evolutionary transitions. Addressing such questions, however, makes high demands of the fossil record (Webster 2019). A more-or-less continu- ous fossil sequence through an adequate period of time would be required to track changes in phenotype and its plasticity, with associated evidence of ancient envi- ronments to test for potentially causal or adaptive factors. Ideally, we would also require time-correlated sequences in different areas to account for habitat variation and dispersal. And each time/space unit should be represented by sufficient fossils of the lineage under study to represent variation within the population and allow statistical testing between samples. Addressing these questions in the fossil record is usually not, therefore, a matter of choosing one’s preferred taxonomic group and getting to work, but carefully selecting a taxon and geological setting that fulfills, or partly fulfills, the above criteria. Moreover, testing these ideas presupposes that it is possible to determine how far morphological change was generated by developmental plasticity or genetic differen- tiation. Often challenging in living species, for fossils it is harder still (Newell, 1947; Dynowski and Nebelsick 2011; Webster 2019). Unlike present-day studies, we cannot undertake field transplants, laboratory manipulation of conditions, breeding experi- ments, or (except in very rare cases) access the genotype. All we have is morphology, normally restricted to hard parts, and sometimes traces of the organism’s activity in life. These challenges, and the solutions that have been proposed to deal with them, will first be surveyed (Section 11.2). We will then explore to what extent fossil data can be brought to bear on the major evolutionary questions where phenotypic plastic- ity has been implicated (Section 11.3). Plasticity in the Fossil Record 269 11.2 IDENTIFYING PHENOTYPIC PLASTICITY IN THE FOSSIL RECORD Many paleontological papers, acknowledging that observed variation might be due either to plasticity or to genetic differentiation, explicitly decline to choose between them. Yet a variety of distinguishing criteria have been proposed (e.g., Lister 1992; McKinney and McNamara 1991; Chauffe and Nichols 1995; Schoch 2014; Jackson 2020), and an account of them illustrates the great diversity of fossil examples in which phenotypic plasticity (often referred to as ecophenotypy in the paleontological litera- ture) has been explored, from protists to humans, and from the earliest known fossils up to the historical period (Box 11.1). Note that in many cases several of the factors listed below are taken together to support the identification of phenotypic plasticity. BOX 11.1 THE GEOLOGICAL TIMESCALE: MYR, MILLIONS OF YEARS AGO Eon Era Period Epoch Start Date (Myr) Holocene 0.012 Quaternary Pleistocene 2.6 Pliocene 5.3 Neogene Cenozoic Miocene 23 Tertiary Oligocene 34 Paleogene Eocene 56 Paleocene 66 Cretaceous 146 Phanerozoic Mesozoic Jurassic 200 Triassic 251 Permian 299 Carboniferous 359 Devonian 416 Paleozoic Silurian 444 Ordovician 488 Cambrian 542 Neoproterozoic Ediacaran 635 Proterozoic Mesoproterozoic Paleoproterozoic 2500 11.2.1 CORRELATION WITH PALEOENVIRONMENTAL VARIATION Fossil species are often found across a range of locations or time-intervals with evidence of variation in factors such as temperature, salinity, water depth, or predation pressure (Figure 11.1). 270 Phenotypic Plasticity & Evolution FIGURE 11.1 An example of the reconstruction of paleoenvironmental variation in time and space from rocks deposited in different settings. The block represents an area of approxi- mately 20 × 10 km in north-central Illinois during Pennsylvanian (Upper Carboniferous) times; vertical scale greatly exaggerated. Algal mound: a mat of algae in shallow seas that aggrades limestone; algal flank: side of algal mound; interdistributary: area between the chan- nels of a delta; intertidal: shore between high and low tides; shoal: sandbanks off the coast; supratidal: shore above high tide. (Reprinted with permission from Hickey, D.R., Journal of Paleontology, 61, 290–311, 1987.) These paleoenvironmental factors can be assessed via a variety of proxies, includ- ing stable isotopes, the composition of the faunal community, and the nature of the enclosing sediment that reflects aspects such as water flow rate and the nature of the ancient substratum. If across samples with constant environment, the phenotype of the target species remained the same, but with observed environmental differences it varied, phenotypic plasticity is suspected, and in many cases a likely adaptive basis for the correlation can be suggested. For example, Witts et al. (2020) examined shell shape in Late Cretaceous ammo- nites (a group of extinct molluscs with coiled shells, related to squid). Tracing the species Hoploscaphites nicolletii across its entire spatial and temporal range, the authors found no directional trend but variations in shell shape correlated with those of paleoenvironmental proxies. Thus, the shells were more compressed in areas of faster water flow where this shape is believed to improve hydrodynamic efficiency, and the authors interpret this as adaptive phenotypic plasticity. In a species